The role and risks of selective adaptation in extreme coral habitats

The alarming rate of climate change demands new management strategies to protect coral reefs. Environments such as mangrove lagoons, characterized by extreme variations in multiple abiotic factors, are viewed as potential sources of stress-tolerant corals for strategies such as assisted evolution and coral propagation. However, biological trade-offs for adaptation to such extremes are poorly known. Here, we investigate the reef-building coral Porites lutea thriving in both mangrove and reef sites and show that stress-tolerance comes with compromises in genetic and energetic mechanisms and skeletal characteristics. We observe reduced genetic diversity and gene expression variability in mangrove corals, a disadvantage under future harsher selective pressure. We find reduced density, thickness and higher porosity in coral skeletons from mangroves, symptoms of metabolic energy redirection to stress response functions. These findings demonstrate the need for caution when utilizing stress-tolerant corals in human interventions, as current survival in extremes may compromise future competitive fitness.


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Behavioural & social sciences Ecological, evolutionary & environmental sciences For a reference copy of the document with all sections, see nature.com/documents/nr-reporting-summary-flat.pdf

Ecological, evolutionary & environmental sciences study design
All studies must disclose on these points even when the disclosure is negative. Porites lutea corals at two different sites (Woody Isles and Low Isles, Australia) were sampled at a depth of 1-1.5 m. Colonies (9-10 per site) of comparable size were sampled with a chisel (5-6 m apart to minimize the potential of sampling clonal genotypes) to obtain small colonies (4-6 cm total length) at both sites. Collected corals were assigned to molecular analysis or skeleton physical property analysis. Four independent samples were obtained for each site for molecular analysis. Multiple tests were performed to assess the physical properties of the coral skeletons. Bulk density and porosity were determined for 5-6 samples per site (3 technical replicates per sample). For hardness, a~1 cm cross section of coral was taken from the center of each sample (same location across samples, n = 3 samples per study site). Tomographic scanning of the skeleton fragments was conducted on n = 3 per site.
The genus Porites is considered a hardy coral taxon and has been documented across extreme mangrove systems globally, making it a good candidate to test the resilience of corals to extreme environmental changes. Porites lutea is an important reef forming species in the Indo-Pacific, and it is a dominant coral at the Woody Isles mangrove lagoon and at the Low Isle reef on the Great Barrier Reef. For this study, we collected from each study site 8 colonies of P. lutea , which we analyzed as representative of the local population living at both Woody and Low Isles.
Corals at the reef and mangrove sites were sampled at a depth of 1-1.5 m. Colonies (9-10 per site) of comparable size were sampled with a chisel (5-6 m apart to minimize the potential of sampling clonal genotypes) to obtain small colonies (4-6 cm total length) at both sites. Sample size was determined in order to have enough replicates per each site (> 3) for all subsequent analyses to be performed (molecular and skeletal). Sensitivity of the location and permitting restrictions limited overcollection, which also shaped the sample size used.
Corals were collected in February 2018 by Emma Camp.
Samples were collected on the 21st February 2018. Independent colonies (> 5 m apart to minimize the potential of sampling clonal genotypes) were collected at each of the two sites (Low Isles reef and Woody Isles mangrove lagoon).
No data were excluded Field-collected samples Experimental design and analyses performed are described in details to facilitate reproducibility of the experimental findings. In addition, all code used and raw data are provided along with the manuscript.
Independent colonies (9-10 per site, > 5 m apart to minimize the potential of sampling clonal genotypes) were haphazardly collected at each site. Per each habitat of origin, colonies were randomly assigned to either molecular analysis (4 per site) or skeleton physical property analysis (5-6 per site).
Coral samples were collected haphazardly within each environment. Blinding was not relevant to this study, since divers had to know in which environment they were going to dive to collect the samples.
Samples were collected during the summer, wet season. Conditions were dry when the corals were collected. Average temperature at Low Isles reef at time of collection. Longterm site data for temperature, pH, oxygen and salinity is The site was accessed by boat to limit any impact to the reef. All coral collections were undertaken in accordance with the Great Barrier Reef Marine Park Authority rules. The collection permit was G18/40023.1 issued to Emma Camp. In accordance with the permit, a limit number of samples, and size of sample were collected to minimize impact on the site. Community consultation, including with traditional owners occurred before th permit was issued.
As described above, we followed all permitting requirements to minimise any impact on the site. Further, coral collections were done by hand to avoid any potential damage from power tools.

No laboratory animals
Porites lutea corals at both Woody Isles and Low Isles (Australia) were sampled at a depth of 1-1.5 m. Colonies (9-10 per site) of comparable size were sampled with a chisel (5-6 m apart to minimize the potential of sampling clonal genotypes) to obtain small colonies (4-6 cm total length) at both sites. Samples were placed in a zip-lock bag containing native seawater to return to the research vessel (< 20 min). Once on the research vessel, colonies were assigned to molecular analysis or skeleton physical property analysis.
Sex information is not relevant here, thus it has not been collected.
Field-collected corals were immediately frozen in liquid nitrogen and maintained at -80°C at the University of Technology Sydney prior to RNA extraction. Samples used for physical property analysis were air dried and stored in protective containers to prevent